Tau-tubulin kinase

Frontiers in Molecular Neuroscience

Volumn 7, Issue 1 APR, 2014, Pages

  Ikezu, Seiko ^a   Ikezu, Tsuneya ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; CDK5; GSK3; Kinase; Neuroinflammation; SCA11; Tau; Tauopathy

Indexed keywords

CALPAIN 1; CASEIN KINASE; CHEMOKINE RECEPTOR CX3CR1; CYCLIN DEPENDENT KINASE 5; F ACTIN; G ACTIN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NITRIC OXIDE SYNTHASE; PEPTIDES AND PROTEINS; PROTEIN P25; PROTEIN P35; PROTEIN VARIANT; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SIALOADHESIN; SODIUM COUPLED GLUCOSE TRANSPORTER; TACROLIMUS; TAU TUBULIN KINASE; TAU TUBULIN KINASE 1; TAU TUBULIN KINASE 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ALZHEIMER DISEASE; ARTICLE; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; HIGH THROUGHPUT SEQUENCING; HUMAN; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SPINOCEREBELLAR DEGENERATION;

EID: 84899703338     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00033     Document Type: Article

References (86)

1. +, Cl(-)-coupled betaine/gamma-amino-butyric acid transporter BGT1 by Tau tubulin kinase 2. Cell. Physiol. Biochem. 32, 334-343. doi: 10.1159/000354441
2. Arioka, M., Tsukamoto, M., Ishiguro, K., Kato, R., Sato, K., Imahori, K., et al. (1993). Tau protein kinase II is involved in the regulation of the normal phosphorylation state of tau protein. J. Neurochem. 60, 461-468. doi: 10.1111/j.1471-4159.1993.tb03173.x
3. Asai, H., Ikezu, S., Woodbury, M. E., Yonemoto, G. M., Cui, L., and Ikezu, T. (2014). Accelerated neurodegeneration and neuroinflammation in transgenic mice expressing P301L tau mutant and tau-tubulin kinase 1. Am. J. Pathol.184, 808-818. doi: 10.1016/j.ajpath.2013.11.026
4. Augustinack, J. C., Schneider, A., Mandelkow, E. M., and Hyman, B. T. (2002). Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. 103, 26-35. doi: 10.1007/s004010100423
5. Bauer, P., Stevanin, G., Beetz, C., Synofzik, M., Schmitz-Hubsch, T., Wullner, U., et al. (2010). Spinocerebellar ataxia type 11 (SCA11) is an uncommon cause of dominant ataxia among French and German kindreds. J. Neurol. Neurosurg. Psychiatry 81, 1229-1232. doi: 10.1136/jnnp.2009.202150
6. Benoit, M., Desnues, B., and Mege, J. L. (2008). Macrophage polarization in bacterial infections. J. Immunol. 181, 3733-3739. doi: 10.1097/QCO.0b013e328344b73e
7. Bhaskar, K., Konerth, M., Kokiko-Cochran, O. N., Cardona, A., Ransohoff, R. M., and Lamb, B. T. (2010). Regulation of tau pathology by the microglial fractalkine receptor. Neuron 68, 19-31. doi: 10.1016/j.neuron.2010.08.023
8. Bouskila, M., Esoof, N., Gay, L., Fang, E. H., Deak, M., Begley, M. J., et al. (2011). TTBK2 kinase substrate specificity and the impact of spinocerebellar-ataxia-causing mutations on expression, activity, localization and development. Biochem. J. 437, 157-167. doi: 10.1042/BJ20110276
9. Brown, G. C. (2007). Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem. Soc. Trans. 35, 1119-1121. doi: 10.1042/BST0351119
10. Brunden, K. R., Ballatore, C., Crowe, A., Smith, A. B. III, Lee, V. M., and Trojanowski, J. Q. (2010). Tau-directed drug discovery for Alzheimer's disease and related tauopathies: a focus on tau assembly inhibitors. Exp. Neurol.223, 304-310. doi: 10.1016/j.expneurol.2009.08.031
11. Cuny, G. D. (2009). Kinase inhibitors as potential therapeutics for acute and chronic neurodegenerative conditions. Curr. Pharm. Des. 15, 3919-3939. doi: 10.2174/138161209789649330
12. Dhavan, R., Greer, P. L., Morabito, M. A., Orlando, L. R., and Tsai, L. H. (2002). The cyclin-dependent kinase 5 activators p35 and p39 interact with the alpha-subunit of Ca2+/calmodulin-dependent protein kinase II and alpha-actinin-1 in a calcium-dependent manner. J. Neurosci. 22, 7879-7891.
13. Edener, U., Kurth, I., Meiner, A., Hoffmann, F., Hubner, C. A., Bernard, V., et al. (2009). Missense exchanges in the TTBK2 gene mutated in SCA11. J. Neurol. 256, 1856-1859. doi: 10.1007/s00415-009-5209-0
14. El Khoury, J., Toft, M., Hickman, S. E., Means, T. K., Terada, K., Geula, C., et al. (2007). Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat. Med. 13, 432-438. doi: 10.1038/nm1555
15. Flotow, H., Graves, P. R., Wang, A. Q., Fiol, C. J., Roeske, R. W., and Roach, P. J. (1990). Phosphate groups as substrate determinants for casein kinase I action. J. Biol. Chem. 265, 14264-14269.
16. Flotow, H., and Roach, P. J. (1989). Synergistic phosphorylation of rabbit muscle glycogen synthase by cyclic AMP-dependent protein kinase and casein kinase I. implications for hormonal regulation of glycogen synthase. J. Biol. Chem. 264, 9126-9128.
17. Galimberti, D., Fenoglio, C., Lovati, C., Venturelli, E., Guidi, I., Corra, B., et al. (2006). Serum MCP-1 levels are increased in mild cognitive impairment and mild Alzheimer's disease. Neurobiol. Aging 27, 1763-1768. doi: 10.1016/j.neurobiolaging.2005.10.007
18. Gebicke-Haerter, P. J. (2001). Microglia in neurodegeneration: molecular aspects. Microsc. Res. Tech. 54, 47-58. doi: 10.1002/jemt.1120
19. Gerhard, A., Trender-Gerhard, I., Turkheimer, F., Quinn, N. P., Bhatia, K. P., and Brooks, D. J. (2006). In vivo imaging of microglial activation with [11C](R)-PK11195 PET in progressive supranuclear palsy. Mov. Disord. 21, 89-93. doi: 10.1002/mds.20668
20. Goetz, S. C., Liem, K. F. Jr., and Anderson, K. V. (2012). The spinocerebellar ataxia-associated gene Tau tubulin kinase 2 controls the initiation of ciliogenesis. Cell 151, 847-858. doi: 10.1016/j.cell.2012.10.010
21. Gong, C. X., Lidsky, T., Wegiel, J., Zuck, L., Grundke-Iqbal, I., and Iqbal, K. (2000). Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. implications for neurofibrillary degeneration in Alzheimer's disease. J. Biol. Chem. 275, 5535-5544. doi: 10.1074/jbc.275.8.5535
22. Gordon, S., and Martinez, F. O. (2010). Alternative activation of macrophages: mechanism and functions. Immunity 32, 593-604. doi: 10.1016/j.immuni.2010.05.007
23. Grammas, P., and Ovase, R. (2001). Inflammatory factors are elevated in brain microvessels in Alzheimer's disease. Neurobiol. Aging 22, 837-842. doi: 10.1016/S0197-4580(01)00276-7
24. Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., and Binder, L. I. (1986). Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U.S.A. 83, 4913-4917. doi: 10.1073/pnas.83.13.4913
25. Hanger, D. P., Betts, J. C., Loviny, T. L., Blackstock, W. P., and Anderton, B. H. (1998). New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry. J. Neurochem. 71, 2465-2476. doi: 10.1046/j.1471-4159.1998.71062465.x
26. Hasegawa, M., Jakes, R., Crowther, R. A., Lee, V. M., Ihara, Y., and Goedert, M. (1996). Characterization of mAb AP422, a novel phosphorylation-dependent monoclonal antibody against tau protein. FEBS Lett. 384, 25-30. doi: 10.1016/0014-5793(96)00271-2
27. Hawasli, A. H., Benavides, D. R., Nguyen, C., Kansy, J. W., Hayashi, K., Chambon, P., et al. (2007). Cyclin-dependent kinase 5 governs learning and synaptic plasticity via control of NMDAR degradation. Nat. Neurosci. 10, 880-886. doi: 10.1038/nn1914
28. Hickman, S. E., Allison, E. K., and El Khoury, J. (2008). Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J. Neurosci. 28, 8354-8360. doi: 10.1523/JNEUROSCI.0616-08.2008
29. Hong, M., Zhukareva, V., Vogelsberg-Ragaglia, V., Wszolek, Z., Reed, L., Miller, B. I., et al. (1998). Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282, 1914-1917. doi: 10.1126/science.282.5395.1914
30. Houlden, H., Johnson, J., Gardner-Thorpe, C., Lashley, T., Hernandez, D., Worth, P., et al. (2007). Mutations in TTBK2, encoding a kinase implicated in tau phosphorylation, segregate with spinocerebellar ataxia type 11. Nat. Genet. 39, 1434-1436. doi: 10.1038/ng.2007.43
31. Hutton, M., Lendon, C. L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., et al. (1998). Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705. doi: 10.1038/31508
32. Ihara, Y., Nukina, N., Miura, R., and Ogawara, M. (1986). Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer's disease. J. Biochem. 99, 1807-1810.
33. Iqbal, K., Grundke-Iqbal, I., Smith, A. J., George, L., Tung, Y. C., and Zaidi, T. (1989). Identification and localization of a tau peptide to paired helical filaments of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 86, 5646-5650. doi: 10.1073/pnas.86.14.5646
34. Ishiguro, K., Omori, A., Sato, K., Tomizawa, K., Imahori, K., and Uchida, T. (1991). A serine/threonine proline kinase activity is included in the tau protein kinase fraction forming a paired helical filament epitope. Neurosci. Lett. 128, 195-198. doi: 10.1016/0304-3940(91)90259-V
35. Ishiguro, K., Omori, A., Takamatsu, M., Sato, K., Arioka, M., Uchida, T., et al. (1992). Phosphorylation sites on tau by tau protein kinase I, a bovine derived kinase generating an epitope of paired helical filaments. Neurosci. Lett.148, 202-206. doi: 10.1016/0304-3940(92)90839-Y
36. Ishizawa, K., and Dickson, D. W. (2001). Microglial activation parallels system degeneration in progressive supranuclear palsy and corticobasal degeneration. J. Neuropathol. Exp. Neurol. 60, 647-657.
37. Janelsins, M. C., Mastrangelo, M. A., Oddo, S., LaFerla, F. M., Federoff, H. J., and Bowers, W. J. (2005). Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer's disease mice. J. Neuroinflammation 2, 23. doi: 10.1186/1742-2094-2-23
38. Jinwal, U. K., Akoury, E., Abisambra, J. F., O'Leary, J. C. III, Thompson, A. D., Blair, L. J., et al. (2013). Imbalance of Hsp70 family variants fosters tau accumulation. FASEB J. 27, 1450-1459. doi: 10.1096/fj.12-220889
39. Johnson, J., Wood, N., Giunti, P., and Houlden, H. (2008). Clinical and genetic analysis of spinocerebellar ataxia type 11. Cerebellum 7, 159-164. doi: 10.1007/s12311-008-0022-3
40. Kiefer, S. E., Chang, C. J., Kimura, S. R., Gao, M., Xie, D., Zhang, Y., et al. (2014). The structure of human tau-tubulin kinase 1 both in the apo form and in complex with an inhibitor. Acta Crystallogr. F Struct. Biol. Commun. 70, 173-181. doi: 10.1107/S2053230X14000144
41. Kitano-Takahashi, M., Morita, H., Kondo, S., Tomizawa, K., Kato, R., Tanio, M., et al. (2007). Expression, purification and crystallization of a human tau-tubulin kinase 2 that phosphorylates tau protein. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63, 602-604. doi: 10.1107/S1744309107028783
42. Kosik, K. S., Joachim, C. L., and Selkoe, D. J. (1986). Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 83, 4044-4048. doi: 10.1073/pnas.83.11.4044
43. Kraemer, B. C., Burgess, J. K., Chen, J. H., Thomas, J. H., and Schellenberg, G. D. (2006). Molecular pathways that influence human tau-induced pathology in Caenorhabditis elegans. Hum. Mol. Genet. 15, 1483-1496. doi: 10.1093/hmg/ddl067
44. Lewis, J., McGowan, E., Rockwood, J., Melrose, H., Nacharaju, P., Van Slegtenhorst, M., et al. (2000). Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet. 25, 402-405. doi: 10.1038/78078
45. Li, G., Yin, H., and Kuret, J. (2004). Casein kinase 1 delta phosphorylates tau and disrupts its binding to microtubules. J. Biol. Chem. 279, 15938-15945. doi: 10.1074/jbc.M314116200
46. Lue, L. F., Rydel, R., Brigham, E. F., Yang, L. B., Hampel, H., Murphy, G. M. Jr., et al. (2001). Inflammatory repertoire of Alzheimer's disease and nondemented elderly microglia in vitro. Glia 35, 72-79. doi: 10.1002/glia.1072
47. Lund, H., Cowburn, R. F., Gustafsson, E., Stromberg, K., Svensson, A., Dahllund, L., et al. (2013). Tau-tubulin kinase 1 expression, phosphorylation and co-localization with phospho-Ser422 tau in the Alzheimer's disease brain. Brain Pathol. 23, 378-389. doi: 10.1111/bpa.12001
48. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002). The protein kinase complement of the human genome. Science 298, 1912-1934. doi: 10.1126/science.1075762
49. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., and Locati, M. (2004). The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686. doi: 10.1016/j.it.2004.09.015
50. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. (2002). Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555. doi: 10.1016/S1471-4906(02)02302-5
51. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Titani, K., et al. (1995a). Proline-directed and non-proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 270, 823-829. doi: 10.1074/jbc.270.2.823
52. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Watanabe, A., et al. (1995b). Hyperphosphorylation of tau in PHF. Neurobiol. Aging 16, 365-371; discussion 371-380. doi: 10.1016/0197-4580(95)00027-C
53. Nakielny, S., Campbell, D. G., and Cohen, P. (1991). The molecular mechanism by which adrenalin inhibits glycogen synthesis. Eur. J. Biochem. 199, 713-722. doi: 10.1111/j.1432-1033.1991.tb16175.x
54. Németh, A. H., Kwasniewska, A. C., Lise, S., Parolin Schnekenberg, R., Becker, E. B., Bera, K. D., et al. (2013). Next generation sequencing for molecular diagnosis of neurological disorders using ataxias as a model. Brain 136, 3106-3118. doi: 10.1093/brain/awt236
55. Pola, R., Flex, A., Gaetani, E., Proia, A. S., Papaleo, P., Giorgio, A. D., et al. (2004). Monocyte chemoattractant protein-1 (MCP-1) gene polymorphism and risk of Alzheimer's disease in Italians. Exp. Gerontol. 39, 1249-1252. doi: 10.1016/j.exger.2004.05.001
56. Qi, H., Yao, C., Cai, W., Girton, J., Johansen, K. M., and Johansen, J. (2009). Asator, a tau-tubulin kinase homolog inDrosophila localizes to the mitotic spindle. Dev. Dyn. 238, 3248-3256. doi: 10.1002/dvdy.22150
57. Reynolds, C. H., Nebreda, A. R., Gibb, G. M., Utton, M. A., and Anderton, B. H. (1997). Reactivating kinase/p38 phosphorylates tau protein in vitro. J. Neurochem. 69, 191-198. doi: 10.1046/j.1471-4159.1997.69010191.x
58. Sato, S., Cerny, R. L., Buescher, J. L., and Ikezu, T. (2006). Tau-tubulin kinase 1 (TTBK1), a neuron-specific tau kinase candidate, is involved in tau phosphorylation and aggregation. J. Neurochem. 98, 1573-1584. doi: 10.1111/j.1471-4159.2006.04059.x
59. Sato, S., Tatebayashi, Y., Akagi, T., Chui, D. H., Murayama, M., Miyasaka, T., et al. (2002). Aberrant tau phosphorylation by glycogen synthase kinase-3beta and JNK3 induces oligomeric tau fibrils in COS-7 cells. J. Biol. Chem. 277, 42060-42065. doi: 10.1074/jbc.M202241200
60. Sato, S., Xu, J., Okuyama, S., Martinez, L. B., Walsh, S. M., Jacobsen, M. T., et al. (2008). Spatial learning impairment, enhanced CDK5/p35 activity, and downregulation of NMDA receptor expression in transgenic mice expressing tau-tubulin kinase 1. J. Neurosci. 28, 14511-14521. doi: 10.1523/JNEUROSCI.3417-08.2008
61. Schols, L., Bauer, P., Schmidt, T., Schulte, T., and Riess, O. (2004). Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis. Lancet Neurol. 3, 291-304. doi: 10.1016/S1474-4422(04)00737-9
62. Semple, B. D., Kossmann, T., and Morganti-Kossmann, M. C. (2010). Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cereb. Blood Flow Metab. 30, 459-473. doi: 10.1038/jcbfm.2009.240
63. Serrano-Pozo, A., Mielke, M. L., Gomez-Isla, T., Betensky, R. A., Growdon, J. H., Frosch, M. P., et al. (2011). Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Am. J. Pathol. 179, 1373-1384. doi: 10.1016/j.ajpath.2011.05.047
64. Simpkins, K. L., Guttmann, R. P., Dong, Y., Chen, Z., Sokol, S., Neumar, R. W., et al. (2003). Selective activation induced cleavage of the NR2B subunit by calpain. J. Neurosci. 23, 11322-11331.
65. Sun, Y. X., Minthon, L., Wallmark, A., Warkentin, S., Blennow, K., and Janciauskiene, S. (2003). Inflammatory markers in matched plasma and cerebrospinal fluid from patients with Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 16, 136-144. doi: 10.1159/000071001
66. Takahashi, M., Tomizawa, K., Sato, K., Ohtake, A., and Omori, A. (1995). A novel tau-tubulin kinase from bovine brain. FEBS Lett. 372, 59-64. doi: 10.1016/0014-5793(95)00955-9
67. Takashima, A., Noguchi, K., Sato, K., Hoshino, T., and Imahori, K. (1993). Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 90, 7789-7793. doi: 10.1073/pnas.90.16.7789
68. Takashima, A., Yamaguchi, H., Noguchi, K., Michel, G., Ishiguro, K., Sato, K., et al. (1995). Amyloid beta peptide induces cytoplasmic accumulation of amyloid protein precursor via tau protein kinase I/glycogen synthase kinase-3 beta in rat hippocampal neurons. Neurosci. Lett. 198, 83-86. doi: 10.1016/0304-3940(95)11964-X
69. Tanos, B. E., Yang, H. J., Soni, R., Wang, W. J., Macaluso, F. P., Asara, J. M., et al. (2013). Centriole distal appendages promote membrane docking, leading to cilia initiation. Genes Dev. 27, 163-168. doi: 10.1101/gad.207043.112
70. Tomizawa, K., Omori, A., Ohtake, A., Sato, K., and Takahashi, M. (2001). Tau-tubulin kinase phosphorylates tau at Ser-208 and Ser-210, sites found in paired helical filament-tau. FEBS Lett. 492, 221-227. doi: 10.1016/S0014-5793(01)02256-6
71. Vazquez-Higuera, J. L., Martinez-Garcia, A., Sanchez-Juan, P., Rodriguez-Rodriguez, E., Mateo, I., Pozueta, A., et al. (2011). Genetic variations in tau-tubulin kinase-1 are linked to Alzheimer's disease in a Spanish case-control cohort. Neurobiol. Aging 32, 550. e5-550. e9. doi: 10.1016/j.neurobiolaging.2009.12.021
72. Vega, I. E., Cui, L., Propst, J. A., Hutton, M. L., Lee, G., and Yen, S. H. (2005). Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates. Brain Res. Mol. Brain Res. 138, 135-144. doi: 10.1016/j.molbrainres.2005.04.015
73. Weingarten, M. D., Lockwood, A. H., Hwo, S. Y., and Kirschner, M. W. (1975). A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. U.S.A. 72, 1858-1862. doi: 10.1073/pnas.72.5.1858
74. Wolozin, B. L., Pruchnicki, A., Dickson, D. W., and Davies, P. (1986). A neuronal antigen in the brains of Alzheimer patients. Science 232, 648-650. doi: 10.1126/science.3083509
75. Worth, P. F., Giunti, P., Gardner-Thorpe, C., Dixon, P. H., Davis, M. B., and Wood, N. W. (1999). Autosomal dominant cerebellar ataxia type III: linkage in a large British family to a 7.6-cM region on chromosome 15q14-21.3. Am. J. Hum. Genet. 65, 420-426. doi: 10.1086/302495
76. Wu, H. Y., Hsu, F. C., Gleichman, A. J., Baconguis, I., Coulter, D. A., and Lynch, D. R. (2007). Fyn-mediated phosphorylation of NR2B Tyr-1336 controls calpain-mediated NR2B cleavage in neurons and heterologous systems. J. Biol. Chem. 282, 20075-20087. doi: 10.1074/jbc.M700624200
77. Wu, H. Y., Yuen, E. Y., Lu, Y. F., Matsushita, M., Matsui, H., Yan, Z., et al. (2005). Regulation of N-methyl-D-aspartate receptors by calpain in cortical neurons. J. Biol. Chem. 280, 21588-21593. doi: 10.1074/jbc.M501603200
78. Xia, M. Q., and Hyman, B. T. (1999). Chemokines/chemokine receptors in the central nervous system and Alzheimer's disease. J. Neurovirol. 5, 32-41. doi: 10.3109/13550289909029743
79. Xu, J., Tsutsumi, K., Tokuraku, K., Estes, K. A., Hisanaga, S. I., and Ikezu, T. (2010a). Actin interaction and regulation of cyclin-dependent kinase 5/p35 complex activity. J. Neurochem. 116, 192-204. doi: 10.1111/j.1471-4159.2010.06824.x
80. Xu, J., Sato, S., Okuyama, S., Swan, R. J., Jacobsen, M. T., Strunk, E., et al. (2010b). Tau-tubulin kinase 1 enhances prefibrillar tau aggregation and motor neuron degeneration in P301L FTDP-17 tau-mutant mice. FASEB J. 24, 2904-2915. doi: 10.1096/fj.09-150144
81. Xue, Y., Wan, P. T., Hillertz, P., Schweikart, F., Zhao, Y., Wissler, L., et al. (2013). X-ray structural analysis of tau-tubulin kinase 1 and its interactions with small molecular inhibitors. ChemMedChem 8, 1846-1854. doi: 10.1002/cmdc.201300274
82. Yamamoto, M., Horiba, M., Buescher, J. L., Huang, D., Gendelman, H. E., Ransohoff, R. M., et al. (2005). Overexpression of monocyte chemotactic protein-1/CCL2 in beta-amyloid precursor protein transgenic mice show accelerated diffuse beta-amyloid deposition. Am. J. Pathol. 166, 1475-1485. doi: 10.1016/S0002-9440(10)62364-4
83. Ye, X., Zeng, H., Ning, G., Reiter, J. F., and Liu, A. (2014). C2cd3 is critical for centriolar distal appendage assembly and ciliary vesicle docking in mammals. Proc. Natl. Acad. Sci. U.S.A. 111, 2164-2169. doi: 10.1073/pnas.1318737111
84. Yoshiyama, Y., Higuchi, M., Zhang, B., Huang, S. M., Iwata, N., Saido, T. C., et al. (2007). Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53, 337-351. doi: 10.1016/j.neuron.2007.01.010
85. Yu, N. N., Yu, J. T., Xiao, J. T., Zhang, H. W., Lu, R. C., Jiang, H., et al. (2011). Tau-tubulin kinase-1 gene variants are associated with Alzheimer's disease in Han Chinese. Neurosci. Lett. 491, 83-86. doi: 10.1016/j.neulet.2011.01.011
86. Zhang, S., Edelmann, L., Liu, J., Crandall, J. E., and Morabito, M. A. (2008). Cdk5 regulates the phosphorylation of tyrosine 1472 NR2B and the surface expression of NMDA receptors. J. Neurosci. 28, 415-424. doi: 10.1523/JNEUROSCI.1900-07.2008